First Detection of TBE Virus in Ticks and Sero-Reactivity in Goats in a Non-Endemic Region in the Southern Part of Switzerland (
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Ticks and Tick-borne Diseases 10 (2019) 868–874 Contents lists available at ScienceDirect Ticks and Tick-borne Diseases journal homepage: www.elsevier.com/locate/ttbdis Original article First detection of TBE virus in ticks and sero-reactivity in goats in a non- endemic region in the southern part of Switzerland (Canton of Ticino) T ⁎ Simona Casati Pagania, , Simona Frigerio Malossab, Christine Klausc, Donata Hoffmannd, Ottavio Berettaa, Nicola Bomio-Pacciorinie, Mario Lazzaroa, Giorgio Merlania, Rahel Ackermannf, Christian Beuretg a Dipartimento della sanità e della socialità, Ufficio del medico cantonale, Via Dogana 16, 6500, Bellinzona, Switzerland b EOC – Dipartimento di medicina di laboratorio, Servizio di microbiologia (SMIC), Via Mirasole 22a, 6500, Bellinzona, Switzerland c Friedrich-Loeffler-Institut, Institute of Bacterial Infections and Zoonoses, Naumburger Str. 96a, 07743, Jena, Germany d Friedrich-Loeffler-Institut, Institute of Diagnostic Virology, Südufer 10, 17493, Greifswald-Insel Riems, Germany e Dipartimento del territorio, Ufficio forestale 4° circondario, Via Antonio Ciseri 13, 6600, Locarno, Switzerland f National Reference Centre for Tick-Transmitted Diseases (NRZK), Labor Spiez, Ausstrasse, 3700, Spiez, Switzerland g Spiez Laboratory, Ausstrasse, 3700, Spiez, Switzerland ARTICLE INFO ABSTRACT Keywords: In Switzerland, tick-borne encephalitis (TBE) is a notifiable human disease with an average of 210 cases per year TBEV in the last 10 years (2008–2017). A national surveillance conducted in 2009 reported a prevalence of 0.46% for Goats tick-borne encephalitis virus (TBEV) detected in ticks, which is in accordance with the prevalences found in Ticks Europe from 0.1%–5%. The Canton of Ticino in the southern part of Switzerland, geographically separated from Ixodes ricinus the rest of the national territory by the Alps, is considered a non-endemic region, as no autochthonous clinical Switzerland cases and no TBEV presence in ticks have ever been reported. In order to understand the epidemiological si- Seroprevalence fi Sentinel host tuation in Ticino, we conducted a large study investigating the TBEV presence in eld-collected Ixodes ricinus ticks and in goat and human sera. Goats and sheep were considered as sentinel hosts showing persistence of antibodies also after 28 months in the absence of symptoms; this longevity supports the data validity to char- acterize an area with the TBEV status. The goat sera collection was composed of a total of 662 samples from 37 flocks. The total seroprevalence was 14.6%. 39 (40%) of the 97 SNT-positive samples showed an antibody titer ≥ 1:120 which indicates recent infection and consequently the probable presence of active foci among the pastures frequented by the goats belonging to 10 flocks. In total, 51 owners participated in the study and all were TBEV antibody-free. A total of 12’052 I. ricinus ticks (nymphs and adults) were collected and 1’371 pools were tested using quantitative real-time RT-PCR. Only one positive pool was reported with a prevalence of 0.35%. Metagenomic analysis revealed that the TBEV strain isolated from the ticks collected in Ticino is closely related to 2 strains coming from the Canton of Valais (99.1% and 98.7% identity, respectively), a neighbouring region of the Canton of Ticino. These two Cantons are close together but separated by high mountains (Alps) and we hypothesize that infected ticks were transported by wild animals from Valais into the Valle Maggia in Ticino where we found positive ticks. In conclusion, our data show for the first time the presence of TBEV in ticks and the related sero- reactivity in goats, confirming the presence of TBEV in the environment of the Canton of Ticino. Further sur- veillance studies will have to be conducted to follow the persistence of TBEV in this region. 1. Introduction carry various pathogens with the potential to generate serious human and animal diseases. In Switzerland, the two most frequent tick-borne Ticks are considered the second most important vector for human human diseases are Lyme borreliosis and tick-borne encephalitis (TBE). diseases worldwide after the mosquitoes (Parola and Raoult, 2001). In The first disease caused by the bacterial species complex Borrelia Europe, the most widespread tick species is Ixodes ricinus, which may burgdorferi sensu lato is spread in Swiss forests up to an altitude of ⁎ Corresponding author at: Dipartimento della sanità e della socialità, Ufficio del medico cantonale, Via Dogana 16, 6500, Bellinzona, Switzerland. E-mail address: [email protected] (S. Casati Pagani). https://doi.org/10.1016/j.ttbdis.2019.04.006 Received 15 November 2018; Received in revised form 28 March 2019; Accepted 10 April 2019 Available online 18 April 2019 1877-959X/ © 2019 Published by Elsevier GmbH. S. Casati Pagani, et al. Ticks and Tick-borne Diseases 10 (2019) 868–874 Fig. 1. Distribution of the positive tick pool (orange star), the seropositive flocks with an antibody titer ≥ 1:120 (active foci, red dot), the seropositive flocks (past infection, orange dot) and the seronegative flocks (grey dot) in Canton of Ticino. The TBEV strains were isolated in two endemic areas in Canton of Valais (blue star) and in a pool of ticks in Valle Maggia (orange star). The Canton of Ticino and the Canton of Valais are separated by high mountains (Alps) partly situated in Italy. The red line shows the game ways between the two Cantons supporting the transfer of the TBEV from Valais to Ticino. 1’500 m (Medlock et al., 2013) overlapping the distribution of I. ricinus. considered as amplifier hosts play an important role in the enzootic In contrast, the tick-borne encephalitis virus (TBEV) shows an irregular transmission cycle of TBEV (Randolph et al., 1999). However, these distribution over a large geographical range with a patchy occurrence hosts develop a short viraemic phase (2-3 days) resulting in a low viral in restricted foci of limited size (Dobler et al., 2011), where the TBEV transmission potential to ticks. An essential element for virus main- circulates among tick and vertebrate populations (Charrel et al., 2004; tenance is the non-viraemic transmission between infected nymphs and Dumpis et al., 1999). non-infected larvae co-feeding on the same host without viraemia In Switzerland, natural foci are defined by registering the numbers (Randolph, 2001). Small animals develop an immune response which of autochthonous human cases and/or detection of the virus in ticks and consists in the development of persistent TBEV-specific antibodies are reported on a map published on the website of the Swiss Federal (Tonteri et al., 2016). Therefore, an alternative and complementary Office of Public Health (www.bag.admin.ch). This map indicates the way to detect TBE foci is the serological approach as demonstrated by areas where vaccination against TBEV is recommended. A national Burri who tested rodents captured at four endemic sites in Switzerland study on the prevalence of TBEV in ticks reported a mean virus pre- (Burri et al., 2012). Other animals like goats and sheep show a regular valence of 0.46% (Gäumann et al., 2010), which is in accordance with persistence of antibodies after subclinical infection. These animals live the prevalence of 0.1%–5% found in Europe (Dumpis et al., 1999; in specific areas over prolonged periods where they eventually acquire Oehme et al., 2002; Randolph, 2001). Another recent study showed the TBEV through repetitive tick bites (Klaus et al., 2012). Therefore, the absence of TBEV in questing I. ricinus ticks collected in urban and flocks are considered as sentinels for the presence of TBEV in a specific suburban areas in Switzerland (Oechslin et al., 2017). The low pre- geographic area, thus helping to better describe the epidemiological valence, the spotted distribution and the irregular circulation of TBEV situation (Klaus et al., 2010b). makes the detection of new foci very expensive and time-consuming In Switzerland, TBE is a notifiable human disease with an average of (Klaus et al., 2010a). In addition, it must be considered that areas with 210 cases per year in the last 10 years (2008–2017) with a peak of 257 TBEV-positive ticks do not always coincide with areas defined by the cases in 2017 (UFSP, 2017). The southern part of Switzerland, precisely human TBE incidence as shown in a country-wide surveillance study in the Canton of Ticino, separated from the rest of the national territory by Switzerland in 2009 with a total of 62’343 I. ricinus ticks collected in the Alps, is considered a non-endemic region, as no autochthonous 145 places (Gäumann et al., 2010). clinical cases have ever been reported. The present study is the first Many aspects remain inexplicable being confronted with a complex report of the presence of TBEV in I. ricinus ticks in this region. As the eco-epidemiological system, characterized by an intricate interplay Canton Ticino was omitted in the already mentioned first national tick between virus, ticks and tick hosts, human exposure (Kunze and ISW, surveillance study in 2009, we conducted a canton-wide study in 2014 2018), and environmental and ecological conditions. Small rodents to elucidate the prevalence of TBEV in I. ricinus ticks in this region. The 869 S. Casati Pagani, et al. Ticks and Tick-borne Diseases 10 (2019) 868–874 Table 1 TBEV-specific antibodies in goats collected in 2014, 2015 and 2016 in 6 districts of the Canton of Ticino. Village District Collection period Total number of sera Total SNT-positive sera SNT Number of SNT samples with an AB titre ≥ 1:120* (flock) Seroprevalence (%) Bellinzona Bellinzona 2015 20 7 35 5 Bellinzona Bellinzona 2016 4 0 0 0 Gudo Bellinzona 2014 12 0 0 0 Isone Bellinzona 2016 3 0 0 0 Medeglia Bellinzona 2015 3 0 0 0 Monte Carasso Bellinzona 2016 2 0 0 0 Rivera Bellinzona 2015 17 0 0 0 S.